What Can We Learn from a Biomimetic Model of Nature's Oxygen-Evolving Complex?

A recently reported synthetic complex with a Mn₄CaO₄ core represents a remarkable structural mimic of the Mn₄CaO₅ cluster in the oxygen-evolving complex (OEC) of photosystem II (Zhang et al., Science 2015, 348, 690). Oxidized samples of the complex show electron paramagnetic resonance (EPR) signals at g ≈ 4.9 and 2, similar to those associated with the OEC in its S₂ state (g ≈ 4.1 from an S = ⁵/₂ form and g ≈ 2 from an S = ¹/₂ form), suggesting similarities in the electronic as well as geometric structure. We use quantum-chemical methods to characterize the synthetic complex in various oxidation states, to compute its magnetic and spectroscopic properties, and to establish connections with reported data. Only one energetically accessible form is found for the oxidized "S₂ state" of the complex. It has a ground spin state of S = ⁵/₂, and EPR simulations confirm it can be assigned to the g ≈ 4.9 signal. However, no valence isomer with an S = ¹/₂ ground state is energetically accessible, a conclusion supported by a wide range of methods, including density matrix renormalization group with full valence active space. Alternative candidates for the g ≈ 2 signal were explored, but no low-spin/low-energy structure was identified. Therefore, our results suggest that despite geometric similarities the synthetic model does not mimic the valence isomerism that is the hallmark of the OEC in its S₂ state, most probably because it lacks a coordinatively flexible oxo bridge. Only one of the observed EPR signals can be explained by a structurally intact high-spin one-electron-oxidized form, while the other originates from an as-yet-unidentified rearrangement product. Nevertheless, this model provides valuable information for understanding the high-spin EPR signals of both the S₁ and S₂ states of the OEC in terms of the coordination number and Jahn-Teller axis orientation of the Mn ions, with important consequences for the development of magnetic spectroscopic probes to study S-state intermediates immediately prior to O-O bond formation.